Interplay between demography and selection: a forward model illuminates the temporal genetic signatures of rapid adaptation in plant pathogens

Abstract

1AbstractThe demography and genetic structure of a population are closely linked. The study of this interplay is crucial, especially for organisms with frequent demographic fluctuations such as pathogen species responsible for emerging diseases. The joint study of demographic variations and genetic evolution of a pathogen population can be achieved by coupling epidemiology and population genetics. This framework is particularly suited to the study of genetic signatures of strong and rapid selective events, such as pathogen adaptation to plant genetic resistances. We have limited knowledge of how these events shape the genetic evolution of pathogens and what would be the typical genetic signatures of strong demographic and selective events on the pathogen population. In this study, we model pathogen population dynamics and genetic evolution at neutral loci to draw a typology of scenarios of eco-evolutionary dynamics. Using a clustering method dedicated to time-series variations, we identify three main scenarios: 1) small variations in the pathogen population size and small changes in genetic structure, 2) a strong founder event on the resistant host that in turn leads to a genetic structure on the susceptible host, and 3) evolutionary rescue that results in a strong founder event on the resistant host, preceded by a bottleneck on the susceptible host. Beyond the selective event itself, the demographic trajectory imposes specific changes in the genetic structure of the pathogen population. Most of these genetic changes are transient, with a signature of resistance overcoming that vanishes in a few years only. Considering time series is therefore of utmost importance for accurate tracking of the evolutionary trajectories of pathogen populations.